Prevalence of Clonorchis sinensis Infection among Residents along 5 Major Rivers in the Republic of Korea

Article information

Korean J Parasitol. 2016;54(2):215-219
Publication date (electronic) : 2016 April 30
doi : https://doi.org/10.3347/kjp.2016.54.2.215
Division of Malaria and Parasite Diseases, Korea National Institute of Health, Korea Centers for Disease Control and Prevention, Cheongju (Osong) 28159, Korea
*Corresponding author (tell74@naver.com)

These authors contributed equally to this work.

Received 2015 July 21; Revised 2016 January 12; Accepted 2016 January 20.

Abstract

Clonorchis sinensis is currently the most important parasite affecting public health problems in the Republic of Korea. We investigated the prevalence of C. sinensis infection among residents living along 5 major rivers in Korea. A total of 42,562 individual stool samples were collected from 37 localities and examined using the formalin-ether sedimentation technique. Helminth eggs were detected in 4,052 (9.5%) residents and 3,586 (8.4%) were infected with C. sinensis. The egg positive rate of C. sinensis in Nakdong, Seomjin, Geum, Yeongsan, and Han River was 11.7%, 9.9%, 6.5%, 3.1%, and 1.0%, respectively. The overall prevalence of clonorchiasis by sex was 11.2% in males and 6.2% in females. The age-prevalence was the highest in the 50-59 years band. It has been reconfirmed that the endemicity of clonorchiasis is higher in southern areas of Korea, especially along Nakdong and Seomjin Rivers. A combination of continuous control programs with health education initiatives is urgently required in these highly endemic areas of clonorchiasis in Korea.

Until the 1970s in the Republic of Korea (Korea), parasitic infections with soil-transmitted intestinal nematodes, such as Ascaris lumbricoides, Trichuris trichiura, and hookworms, were highly prevalent [1,2]. Since 1971, nationwide surveys have been conducted every 5-7 years in order to estimate the infection status of intestinal helminth parasites until 2004 [3]. In the first 1971 survey, the overall prevalence was 84.3%, and by 2004, the rate had dramatically decreased to 3.7%. The rapid decrease in the overall prevalence of intestinal parasites over the past several decades has been attributed mainly to nationwide control programs and health education initiatives undertaken by the Korean government along with improvements in the living conditions and quality of life in Korea [4]. Despite the remarkable decrease of soil-transmitted nematode infections, the prevalence of fish-borne trematode infections such as clonorchiasis and metagonimiasis has still remained to be relatively high [5].

The liver fluke, C. sinensis, is the most important helminth in Korea these days, and clonorchiasis has been known as the cause of biliary pathogenesis, i.e., inflammation, dilatation, wall thickening, mucosal hyperplasia, liver cirrhosis, and even cholangiocarcinoma [6-8]. Among human diseases caused by parasites, clonorchiasis is ranked at the first due to its social, economic, and public health impacts in Korea. Clonorchiasis is endemic in most of the major river basins of Korea [9]. In 1981, the egg positive rates of people living in those river basins differed considerably; 40.2% in Nakdong River, 30.8% in Yeongsan River, 17.3% in Seomjin River, 15.7% in Han River, 15.9% in Tamjin River, and 12.0% in Geum River [10]. However, in 2007, the positive rates of C. sinensis in Nakdong, Seomjin, Yeongsan, Geum, and Han Rivers were 12.2%, 9.5%, 3.3%, 3.0%, and 1.0%, respectively [11]. Although the infection rates of C. sinensis in these major rivers decreased considerably over the past 20 years, clonorchiasis continues to persist and is currently considered as the most important helminthiasis in Korea.

In this study, we investigated the infection status of populations identified to be at risk of clonorchiasis, notably among residents living along 5 major rivers. The surveyed areas consisted of 37 counties, which are located in the vicinity of the Han, Geum, Yeongsan, Seomjin, and Nakdong Rivers, Korea. A total of 42,562 fecal specimens were collected from residents of these regions using a random household sampling method from February to November 2008 (Fig. 1). Stool specimens in plastic containers (1/person) collected in individual survey areas were transferred to the laboratory of National Institute of Health, and then examined by means of the formalin-ether sedimentation technique. Microscopic examinations were performed twice by well-trained technicians. The egg positive rate was estimated by arithmetic means. The egg positive individuals were treated with either praziquantel or other appropriate anti-parasitic drugs at the end of the study.

Fig. 1.

Surveyed areas along 5 major rivers, the Republic of Korea.

More than 10 species of helminth eggs were detected in 4,052 (9.5%) stool samples (Table 1). Eggs of C. sinensis were found in 3,586 (8.4%) fecal specimens of residents. The prevalence of clonorchiasis was highest in residents of Nakdong River (11.7%), followed by Seomjin River (9.9%), Geum River (6.5%), Yeongsan River (3.1%), and Han River (1.0%). Especially, Gyeongju-si (city) had the highest rate of 25.9%, followed by Hadong-gun of 21.9%, which were located in the mid- or downstream of Nakdong and Seomjin Rivers, respectively. Egg positive rates by surveyed areas are shown in Table 2.

Positive rates of parasite eggs by fecal examination in residents along 5 major rivers

Prevalence of overall intestinal parasites and C. sinensis according to localities and river basins

The overall prevalence of clonorchiasis by sex was 11.2% in males and 6.2% in females (Table 3). The egg positive rate by age group was highest in the 50-59 age band, followed by the forties (8.9%), sixties (8.8%), seventies (7.8%), thirties (5.7%), over 80 (5.2%), twenties (2.2%), and below 19 (1.0%) (Table 4).

Positive rate of C. sinensis according to gender and river basins

Prevalence of C. sinensis eggs according to age groups and river basins

The present study provided the prevalence of C. sinensis infection among residents living along 5 major rivers of Korea and confirmed the high endemicity of C. sinensis infection in southern localities. Although the prevalence of clonorchiasis along the major rivers appears to decline over the past decade, we identified that Nakdong and Seomjin Rivers are still highly endemic regions in common with previous studies; a national survey undertaken in 1981 reported that the egg positive rates of people living along these major river basins were 40.2% in Nakdong River, 30.8% in Yeongsan River, 17.3% in Seomjin River, 15.7% in Han River, 15.9% in Tamjin River, and 12.0% in Geum River [10]. Also, in 2006, the egg positive rates of C. sinensis observed in the river basins of Nakdong, Seomjin, Yeongsan, and Geum were 17.1%, 11.2%, 5.5%, and 4.6%, respectively [9]. In addition, our results showed that the positive rates of overall intestinal parasites and C. sinensis in residents along 5 major rivers was 9.5% and 8.4%, respectively. The 9.5% prevalence of overall intestinal parasites is 2-fold higher than the national intestinal helminth prevalence of 3.7% in 2004 [3].

The infection status of C. sinensis according to age groups appears to be a typical pattern for C. sinensis infection, reaching a peak at the age groups of 40-49 and 50-59 years. These results suggest that the eating habit of raw fishes containing C. sinensis metacercariae is a deeply rooted traditional custom among residents living in rural and riverside areas. As well, the higher prevalence in males than in females may be caused by frequent alcohol consumption and raw freshwater fish intake with increasing activities such as fishing that are mostly carried out by men.

While not conceptually new, our results provided the basic data and important information regarding the prevalence of clonorchiasis in high risk regions in Korea and are valuable for providing control strategies and medication of clonorchiasis patients in these areas.

Acknowledgements

This study was supported by parasitic disease surveillance and control program of the National Institute of Health, Ministry of Health and Welfare, Republic of Korea (NIH-4800-4847-311).

Notes

We have no conflict of interest related to this work.

References

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Article information Continued

Fig. 1.

Surveyed areas along 5 major rivers, the Republic of Korea.

Table 1.

Positive rates of parasite eggs by fecal examination in residents along 5 major rivers

Parasite species No. positive cases (%)
Overall intestinal parasites 4,052 (9.5)
Helminths
Clonorchis sinensis 3,586 (8.4)
Metagonimus spp. 411 (1.0)
Trichuris trichiura 63 (0.1)
Echinostoma spp. 12 (0.03)
 Hookworm 5 (0.01)
Ascaris lumbricoides 4 (0.01)
Gymnophalloides seoi 4 (0.01)
Strongyloides stercolalis 4 (0.01)
Trichostrongylus orientalis 1 (0.002)
Diphyllobothrium sp. 1 (0.002)
Co-infection
C. sinensis+Metagonimus spp. 78 (0.18)
C. sinensis+Echinostoma spp. 7 (0.02)
C. sinensis+T. trichiura 5 (0.01)

Table 2.

Prevalence of overall intestinal parasites and C. sinensis according to localities and river basins

River basins Locality No. of examination No. of positive (%) No. of cumulative positive (%) C. sinensis (%)
Han river Hongcheon-gun 1,016 22 (2.2) 22 (2.2) 16 (1.6)
Inje-gun 1,265 15 (1.2) 15 (1.2) 8 (0.6)
Yanggu-gun 1,025 9 (0.9) 9 (0.9) 4 (0.4)
Yeongwol-gun 1,349 35 (2.6) 37 (2.7) 19 (1.4)
Subtotal 4,655 81 (1.7) 83 (1.8) 47 (1.0)
Geum river Buyeo-gun 1,433 47 (3.3) 47 (3.3) 40 (2.8)
Daejeon-si 1,075 42 (3.9) 42 (3.9) 40 (3.7)
Geumsan-gun 1,209 61 (5.0) 62 (5.1) 53 (4.4)
Gongju-si 1,016 48 (4.7) 48 (4.7) 47 (4.6)
Muju-gun 1,708 204 (11.9) 208 (12.2) 190 (11.1)
Yeongdong-gun 287 74 (25.8) 78 (27.2) 68 (23.7)
Subtotal 6,728 476 (7.1) 485 (7.2) 438 (6.5)
Yeongsan river Hampyeong-gun 1,144 47 (4.1) 52 (4.5) 29 (2.5)
Muan-gun 1,267 83 (6.6) 83 (6.6) 32 (2.5)
Naju-si 1,271 54 (4.2) 54 (4.2) 45 (3.5)
Yeongam-gun 1,041 48 (4.6) 48 (4.6) 40 (3.8)
Subtotal 4,723 232 (4.9) 237 (5.0) 146 (3.1)
Seomjin river Boseong-gun 1,200 141 (11.8) 148 (12.3) 123 (10.3)
Gokseong-gun 1,650 169 (10.2) 178 (10.8) 137 (8.3)
Gwangyang-si 1,394 148 (10.6) 149 (10.7) 86 (6.2)
Hadong-gun 1,065 281 (26.4) 306 (28.7) 233 (21.9)
Imsil-gun 1,074 66 (6.1) 68 (6.3) 57 (5.3)
Suncheon-si 1,162 136 (11.7) 144 (12.4) 112 (9.6)
Subtotal 7,545 941 (12.5) 993 (13.2) 748 (9.9)
Nakdong river Andong-si 1,932 258 (13.4) 261 (13.5) 242 (12.5)
Bonghwa-gun 936 20 (2.1) 20 (2.1) 16 (1.7)
Changnyeong-gun 1,044 147 (14.1) 149 (14.3) 141 (13.5)
Changwon-si 851 58 (6.8) 58 (6.8) 56 (6.6)
Geochang-gun 1,256 63 (5.0) 64 (5.1) 61 (4.9)
Gimhae-si 184 6 (3.3) 6 (3.3) 6 (3.3)
Gyeongju-si 710 185 (26.1) 185 (26.1) 184 (25.9)
Haman-gun 1,142 121 (10.6) 122 (10.7) 111 (9.7)
Hapcheon-gun 1,142 184 (16.1) 189 (16.5) 180 (15.8)
Jinju-si 1,020 137 (13.4) 140 (13.7) 134 (13.1)
Miryang-si 1,603 291 (18.2) 294 (18.3) 268 (16.7)
Sancheong-gun 1,365 226 (16.6) 228 (16.7) 222 (16.3)
Sangju-si 1,067 91 (8.5) 92 (8.6) 86 (8.1)
Uiryeong-gun 955 115 (12.0) 115 (12.0) 112 (11.7)
Yecheon-gun 1,314 152 (11.6) 152 (11.6) 151 (11.5)
Yeongdeok-gun 1,253 154 (12.3) 162 (12.9) 125 (10.0)
Yeongyang-gun 1,137 114 (10.0) 114 (10.0) 112 (9.9)
Subtotal 18,911 2,322 (12.3) 2,351 (12.4) 2,207 (11.7)
Total 42,562 4,052 (9.5) 4,149 (9.7) 3,586 (8.4)

Table 3.

Positive rate of C. sinensis according to gender and river basins

River basins No. of positive / No. examined (%)
Male Female Total
Han river 32/2,518 (1.3) 15/2,137 (0.7) 47/4,655 (1.0)
Geum river 307/3,076 (10.0) 131/3,628 (3.6) 438/6,728 (6.5)
Yeongsan river 84/1,915 (4.4) 62/2,808 (2.2) 146/4,723 (3.1)
Seomjin river 422/3,221 (13.1) 326/4,324 (7.5) 748/7,545 (9.9)
Nakdong river 1,306/8,555 (15.3) 901/10,327 (8.7) 2,207/18,911 (11.7)
Total 2,151/19,285 (11.2) 1,435/23,224 (6.2) 3,586/42,562 (8.4)

Table 4.

Prevalence of C. sinensis eggs according to age groups and river basins

River basins No. of positive / No. of examined (%)
Total 1-19 20-29 30-39 40-49 50-59 60-69 70-79 80-
Han river 47/4,655 1/242 7/719 3/327 11/652 17/965 4/917 4/706 0/115
(1.0) (0.4) (1.0) (0.9) (1.7) (1.8) (0.4) (0.6) (0.0)
Geum river 438/6,728 2/302 5/163 7/342 48/738 127/1,330 122/1,746 107/1,638 15/390
(6.5) (0.7) (3.1) (2.0) (6.5) (9.5) (7.0) (6.5) (3.8)
Yeongsan river 146/4,723 0/56 0/56 3/103 18/378 37/893 48/1,531 35/1,428 4/261
(3.1) (0.0) (0.0) (2.9) (4.8) (4.1) (3.1) (2.5) (1.5)
Seomjin river 748/7,545 6/225 11/116 29/276 77/642 152/1,097 203/2,073 187/2,265 34/626
(9.9) (2.7) (9.5) (10.5) (12.0) (13.9) (9.8) (8.3) (5.4)
Nakdong river 2,207/18,911 3/377 6/235 49/558 224/1,815 534/3,773 666/5,523 517/4,880 69/938
(11.7) (0.8) (2.6) (8.8) (12.3) (14.2) (12.1) (10.6) (7.4)
Total 3,586/42,562 12/1,202 29/1,289 91/1,606 378/4,225 867/8,058 1,043/11,790 850/10,917 122/2,330
(8.4) (1.0) (2.2) (5.7) (8.9) (10.8) (8.8) (7.8) (5.2)